Prevalence of macular abnormalities identified only by optical coherence tomography in Brazilian patients with cataract

Prevalence of macular abnormalities identified only by optical coherence tomography in Brazilian patients with cataract

915 ARTICLE Prevalence of macular abnormalities identified only by optical coherence tomography in Brazilian patients with cataract Wanessa P. Pinto...

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ARTICLE

Prevalence of macular abnormalities identified only by optical coherence tomography in Brazilian patients with cataract Wanessa P. Pinto, MD, Laura P. Rabello, MD, Marcelo C. Ventura, MD, PhD, Camilla S. Rocha, BS, Bruna V. Ventura, MD, PhD

Purpose: To assess the prevalence of macular abnormalities not suspected by the biomicroscopic fundus examination and identified only by macular optical coherence tomography (OCT) in the preoperative evaluation for cataract surgery in a large series of Brazilian patients. Setting: Private practice, Recife, Brazil. Design: Retrospective case series. Methods: All eyes that had cataract surgery by the same physician between August 2014 and July 2016 were eligible. Excluded were eyes with a previous diagnosis of macular abnormalities, with a suspicious biomicroscopic fundus examination, and without OCT results. Based on the preoperative macular OCT, patients were divided into the following 2

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ver the years, the progress in phacoemulsification and intraocular lens technology has decreased the risk and augmented the performance of cataract surgery. This has led to increasingly high patient expectations regarding visual outcomes. To meet these expectations, it is necessary to perform a high-quality procedure and to know beforehand whether the patient has an underlying ocular condition that might limit the visual gain.1,2 Historically, macular alterations have been screened for in the preoperative evaluation for cataract surgery by a biomicroscopic fundus examination. Even though this is economically viable, previous studies3–5 have shown that some patients with macular abnormalities present with a normal clinical examination. When these alterations are not identified before surgery, the patient’s expectation might not be met because they were not realistically established.

groups: those with a normal OCT and those with an abnormal OCT.

Results: Nine hundred fifty-two eyes (614 patients) were included in the study. Macular OCT identified abnormalities in 47 eyes (4.9%) of 44 patients (7.2%). Thirty-one eyes (3.3%) had epiretinal membrane, 7 (0.7%) had age-related macular degeneration, 4 (0.4%) had intraretinal cysts, 4 (0.4%) had a lamellar hole, and 1 (0.1%) had a macular hole. Patients with an abnormal OCT had a statistically significant higher mean age (P Z .004). Conclusion: In the preoperative evaluation for cataract surgery in Brazilian patients, 7.2% of those with a normal biomicroscopic fundus examination had macular abnormalities that were identified only by OCT. J Cataract Refract Surg 2019; 45:915–918 Q 2019 ASCRS and ESCRS

A prior study that included 155 Pakistani patients with normal fundus examinations3 reported macular pathologies identified by optical coherence tomography (OCT) in 10.9% of patients. Thus, in that population, 1 in every 9 patients would have had phacoemulsification without knowing about their macular abnormality unless they had an OCT assessment. The purpose of the present study was to assess the prevalence of macular abnormalities not suspected by the biomicroscopic fundus examination and identified only on macular OCT in the preoperative evaluation for cataract surgery in a large series of Brazilian patients. PATIENTS AND METHODS This retrospective study included all patients who had cataract surgery performed by the same physician (M.C.V.) at HOPE Eye Hospital, Recife, Brazil, between August 2014 and July 2016.

Submitted: November 29, 2018 | Final revision submitted: January 17, 2019 | Accepted: January 17, 2019 From the Altino Ventura Foundation (Pinto, Rabello, M.C. Ventura, Rocha, B.V. Ventura) and HOPE Eye Hospital (Rabello, M.C. Ventura, B.V. Ventura), Recife, Pernambuco, Brazil. Presented at the ASCRSASOA Annual Meeting, Washington DC, USA, April 2018. Corresponding author: Bruna V. Ventura, MD, PhD, Altino Ventura Foundation, Rua do Progresso, 71, Boa Vista, Recife (PE), 50070-020, Brazil. Email: brunaventuramd@ gmail.com. Q 2019 ASCRS and ESCRS Published by Elsevier Inc.

0886-3350/$ - see frontmatter https://doi.org/10.1016/j.jcrs.2019.01.022

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MACULAR ABNORMALITIES IDENTIFIED ONLY BY OCT

The study followed the guidelines of the tenets of the Declaration of Helsinki and was approved by the Ethics Committee, Altino Ventura Foundation. The patients’ medical records were reviewed to obtain demographic data and the results of the preoperative consultation. In the institution, the preoperative evaluation for cataract surgery includes slitlamp biomicroscopy (which assesses the anterior segment and the ocular fundus), dilated fundus examination with an indirect binocular ophthalmoscope, optical biometry, Placido-based corneal topography, specular microscopy, corneal pachymetry, and macular OCT, the latter performed using the Avanti spectral-domain OCT (SD-OCT) device (Optovue, Inc.) or the Spectralis HRACOCT device (Heidelberg Engineering, Inc.). Excluded were eyes with a previous diagnosis of macular abnormality and those with a suspicious biomicroscopic fundus examination in the preoperative evaluation; eyes with media opacity that precluded a macular OCT examination were also excluded. Thus, we included all eyes that had cataract surgery without a previous diagnosis of macular abnormality, that had a normal biomicroscopic fundus examination and an OCT obtained in the preoperative evaluation for cataract surgery. Based on the preoperative macular OCT, patients included in the study were divided into the following 2 groups: those with a normal OCT and those with macular abnormalities shown by the OCT in at least 1 eye. An abnormal OCT was defined by the presence of epiretinal membrane (ERM), age-related macular degeneration (AMD), lamellar hole, macular hole, cystoid macular edema, intraretinal cysts, or subretinal neovascular membrane. Statistical analysis was performed using SPSS software (version 24.0, IBM Corp.). Categorical variables are expressed as absolute and relative frequencies. Continuous variables are expressed as the mean G SD and the minimum and maximum values. The chi-square test and the Mann-Whitney test were used to verify statistical significance. A P value of less than 0.05 was used to reject the null hypothesis.

RESULTS The study comprised 1101 eyes of 690 patients. Thirty-eight eyes (3.5%) of 27 patients (3.9%) were excluded from the study because of a previous diagnosis of macular abnormalities, 70 eyes (6.4%) of 45 patients (6.5%) were excluded for a suspicious biomicroscopic fundus examination in the preoperative evaluation, and 41 eyes (3.7%) of 25 patients (3.6%) were excluded because media opacity precluded OCT image acquisition. Thus, 952 eyes of 614 patients were included in the study. The mean age of the patients was 67.4 G 8.7 years (range 24 to 90 years). Three hundred eighty-four patients (62.5%) were women, 357 (58.1%) had systemic arterial hypertension, 151 (24.6%) had diabetes mellitus, and 52 (8.4%) had a history of heart disease. Macular OCT identified abnormalities in 47 eyes (4.9%) of 44 patients (7.2%). Table 1 compares the demographic data of patients with a normal macular OCT with data of patients with an abnormal examination. With regard to the identified macular abnormalities, 31 eyes (3.3%) had ERM, 7 (0.7%%) had AMD, 4 (0.4%) had intraretinal cysts, 4 (0.4%) had a lamellar hole, and 1 (0.1%) had a macular hole (Figure 1). Patients with macular abnormalities identified only by macular OCT had a statistically significant higher mean age than those who had a normal tomographic examination Volume 45 Issue 7 July 2019

Table 1. Comparison of the demographic data of patients with a normal macular OCT examination and those with an abnormal OCT examination. Characteristic Age (y) Mean G SD Range Female, n (%) Arterial hypertension, n (%) Diabetes mellitus, n (%) Heart disease, n (%)

Normal OCT Abnormal OCT (570 Patients) (44 Patients) P Value 67.1 G 8.7 24, 89 357 (62.6) 333 (58.4) 139 (24.4) 49 (8.6)

71.2 G 7.8 54, 90 27 (61.4) 24 (54.5) 12 (27.3) 3 (6.8)

.004* .867† .616† .668† 1.000†

OCT Z optical coherence tomography *Mann-Whitney test † Chi-square test

(P Z .004). There was no statistically significant difference between the 2 groups in any other studied variable. DISCUSSION Macular OCT is a noninvasive, safe, and painless examination that has great accuracy in diagnosing macular abnormalities.4–6 Because identifying these alterations in the preoperative period is important to titrate patients’ expectations and for surgical planning (eg, to determine whether a patient is a good candidate for a presbyopia-correcting intraocular lens), some authors have advocated the inclusion of macular OCT in the evaluation for cataract surgery.3–6 However, a biomicroscopic fundus examination has been the accepted standard of care.3 To assess the benefit of incorporating macular OCT in the preoperative evaluation for cataract surgery, we evaluated the prevalence of macular abnormalities that would have not been identified preoperatively based solely on the biomicroscopic fundus examination in a large series of Brazilian patients.

Figure 1. Spectral-domain optical coherence tomography showing epiretinal membrane (A), lamellar hole (B), and age-related macular degeneration (C).

MACULAR ABNORMALITIES IDENTIFIED ONLY BY OCT

Seven percent of the patients in our study had macular alterations that only OCT identified, which means that for every 14 patients scheduled for cataract surgery, 1 would have had an undiagnosed macular abnormality if the screening were exclusively performed using findings from the biomicroscopic fundus examination. Similarly, Zafar et al.3 reported a 10.9% prevalence of macular alteration among Pakistani patients with a normal clinical examination who were scheduled for routine cataract surgery. Another study5 enrolled 98 Brazilian cataract patients and did not exclude those with a previous clinical diagnosis of macular disease. The preoperative OCT increased the detection of macular abnormalities to 21.4% of patients versus the 11.2% indicated only by the fundus examination. These previous papers corroborate our findings, indicating the importance of incorporating macular OCT in the preoperative evaluation for surgery. In addition to identifying and documenting the macular abnormality in this scenario, OCT is also important for follow-up after surgery. Recently, a swept-source OCT (SS-OCT)–based biometry device (IOLMaster 700, Carl Zeiss Meditec AG) was made commercially available. It uses SS-OCT to obtain biometric data and provides a small central 1.0 mm zone macular scan, which is used to verify eye fixation. Hirnschall et al.6 evaluated its performance in detecting macular abnormalities in cataract patients and compared with that of the Fourier-domain RTVue OCT device (Optovue, Inc.). Even though the SS-OCT device was effective in identifying some patients with central macular pathologies, its lower resolution and small scan size resulted in misdiagnosis in others. Its sensitivity varied from 42% to 68% depending on the observer. Thus, it did not perform as well as the Fourier-domain device, suggesting that it should not be used as a substitute for conventional OCT devices in screening for macular abnormalities in cataract patients. In the present study, the most common macular abnormality identified only by OCT was ERM (3.3%), followed by AMD (0.7%), both of which can negatively impact visual prognosis after cataract surgery.5 Our study is in agreement with that of Huang et al.7 who reported ERM as the leading cause of occult macular abnormality in a large series of Chinese patients with cataract. In the study by Zafar et al.,3 AMD had a slightly higher prevalence than ERM (3.2% versus 2.6%), whereas Moreira Neto et al.5 reported a bigger difference in the prevalence of these etiologies (AMD 6.9% and ERM 3.5%; these percentages were calculated by excluding the 11 eyes with an abnormal fundus examination from their study sample). The disparity between these papers is possibly due to the different studied population and sample size.8,9 In our study, when comparing the demographic data of patients with and without macular abnormalities identified only by OCT, we found that the patient’s mean age was statistically higher in those with occult macular disease. This agrees with results in previous studies that described an increase in the prevalence of retinal diseases as patients age.9–11 The other variables we studied did not have a correlation with occult macular alteration, differing from the

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findings of Klein et al.,4 who reported statistically more macular abnormalities in men and in patients with heart disease. This difference might be the result of the population that was studied. Because eyes with a biomicroscopic suspicion of macular alteration and those with a previous diagnosis of macular disease were excluded from the studies, we cannot eliminate the possibility that we coincidently excluded more male patients and patients with cardiopathology who did not meet our inclusion criteria. Also, the populations were different (patients in the United States versus Brazilian patients), and this might have played a role because the patients’ diet and other modifiable risk factors are reported to be related to the prevalence of some macular abnormalities.12 The main limitation of our study is its retrospective nature and all the drawbacks associated with this design. Furthermore, 2 OCT devices were used in the patients’ preoperative assessment. Although at first this may seem to be a limitation, both devices use SD-OCT technology and have been used extensively in previous studies to assess macular abnormalities.5,13,14 In summary, in the preoperative evaluation for cataract surgery in a large series of Brazilian patients, 7.2% of those with a normal biomicroscopic fundus examination had macular abnormalities that were identified only on OCT. Thus, 1 in every 14 patients having cataract surgery would have had an undiagnosed macular abnormality if the screening were based exclusively on the fundus examination.

WHAT WAS KNOWN  The preoperative identification of macular disease is important to titrate patients’ surgical expectations and to guide intraocular lens choice.  Historically, macular abnormalities have been screened in the preoperative evaluation for cataract surgery by biomicroscopic fundus examination. However, some patients with macular abnormalities present with a normal clinical examination.

WHAT THIS STUDY ADDS  In a large series of Brazilian cataract patients, macular optical coherence tomography identified 7.2% of patients with underlying macular diseases that had been undiagnosed based on the preoperative biomicroscopic fundus examination.

REFERENCES 1. Bozorg S, Pineda R. Cataract and keratoconus: minimizing complications in intraocular lens calculations. Semin Ophthalmol 2014; 29:376–379 2. Schaub F, Adler W, Enders P, Koenig MC, Koch KR, Cursiefen C, Kirchhof B, Heindl LM. Preexisting epiretinal membrane is associated with pseudophakic cystoid macular edema. Graefes Arch Clin Exp Ophthalmol 2018; 256:909–917 3. Zafar S, Siddiqui MAR, Shahzad R, Shahzad MH. Swept-source optical coherence tomography to screen for macular pathology in eyes having routine cataract surgery. J Cataract Refract Surg 2017; 43:324–332

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4. Klein BR, Brown EN, Casden RS. Preoperative macular spectral-domain optical coherence tomography in patients considering advancedtechnology intraocular lenses for cataract surgery. J Cataract Refract Surg 2016; 42:537–541 nior CA, Moreira AT. Optical coherence to5. Moreira Neto CA, Moreira Ju mography in patients undergoing cataract surgery. Arq Bras Oftalmol 2015; 78:241–245 6. Hirnschall N, Leisser C, Radda S, Maedel S, Findl O. Macular disease detection with a swept-source optical coherence tomography-based biometry device in patients scheduled for cataract surgery. J Cataract Refract Surg 2016; 42:530–536 7. Huang X, Zhang Z, Wang J, Meng X, Chen T, Wu Z. Macular assessment of preoperative optical coherence tomography in ageing Chinese undergoing routine cataract surgery. Sci Rep 2018; 8:5103 8. Aung KZ, Makeyeva G, Adams MK, Chong EW-T, Busija L, Giles GG, English DR, Hopper J, Baird PN, Guymer RH, Robman LD. The prevalence and risk factors of epiretinal membranes; the Melbourne Collaborative Cohort Study. Retina 2013; 33:1026–1034 9. Ng CH, Cheung N, Wang JJ, Islam AFM, Kawasaki R, Meuer SM, Cotch MF, Klein BEK, Klein R, Wong TY. Prevalence and risk factors for epiretinal membrane in a multi-ethnic United States population. Ophthalmology 2011; 118:694–699 10. Ye H, Zhang Q, Liu X, Cai X, Yu W, Yu S, Wang T, Lu W, Li X, Hu Y, Yang B, Zhao P. Prevalence and associations of epiretinal membrane in an elderly urban Chinese population in China: the Jiangning Eye Study. Br J Ophthalmol 2015; 99:1594–1597 11. Anastasopoulos E, Haidich AB, Coleman AL, Wilson MR, Harris A, Yu F, Koskosas A, Pappas T, Keskini C, Kalouda P, Karkamanis G, Topouzis F. Risk factors for age-related macular degeneration in a Greek population: the Thessaloniki Eye Study. Ophthalmic Epidemiol 2018; 25:457–469

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12. Piermarocchi S, Tognetto D, Piermarocchi R, Masetto M, Monterosso G, Segato T, Cavarzeran F, Turrini A, Peto T, for the PAMDI Study Group. Risk Factors and age-related macular degeneration in a Mediterraneanbasin population: the PAMDI (Prevalence of Age-Related Macular Degeneration in Italy) Study - report 2. Ophthalmic Res 2016; 55:111–118 13. Ichikawa Y, Imamura Y, Ishida M. Inner nuclear layer thickness, a biomarker of metamorphopsia in epiretinal membrane, correlates with tangential retinal displacement. Am J Ophthalmol 2018; 193:20–27 14. Schlegl T, Waldstein SM, Bogunovic H, Endstraßer F, Sadeghipour A, Philip A-M, Podkowinski D, Gerendas BS, Langs G, Schmidt-Erfurth U. Fully automated detection and quantification of macular fluid in OCT using deep learning. Ophthalmology 2018; 125:549–558

Disclosures: Dr. B.V. Ventura is a consultant to Alcon Laboratories, Inc. and Johnson & Johnson Vision, Inc. None of the other authors has a financial or proprietary interest in any material or method mentioned.

First author: Wanessa P. Pinto, MD Altino Ventura Foundation, Recife, Pernambuco, Brazil